Structural basis for distinct binding properties of the human galectins to Thomsen-Friedenreich antigen

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Bian, Cheng Feng ^a,b   Zhang, Ying ^a   Sun, Hui ^c   Li, De Feng ^a   Wang, Da Cheng ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; GALECTIN 1; GALECTIN 3; THOMSEN FRIEDENREICH ANTIGEN; UNCLASSIFIED DRUG; CARBOHYDRATE; THOMSEN-FRIEDENREICH ANTIGEN; TUMOR ANTIGEN;

ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; BINDING AFFINITY; CARBOHYDRATE RECOGNITION DOMAIN; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; MUTAGENESIS; PROTEIN DOMAIN; STEREOSPECIFICITY; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; CHEMICAL MODEL; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY; SURFACE PLASMON RESONANCE; X RAY CRYSTALLOGRAPHY;

BASIDIOMYCOTA;

AMINO ACID SEQUENCE; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; CARBOHYDRATES; CRYSTALLOGRAPHY, X-RAY; GALECTIN 1; GALECTIN 3; HUMANS; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID; SURFACE PLASMON RESONANCE;

EID: 80052949203     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025007     Document Type: Article

References (38)

1. Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, et al. (1994) Galectins: a family of animal beta-galactoside-binding lectins. Cell 76: 597-598.
2. Lahm H, André S, Hoeflich A, Kaltner H, Siebert HC, et al. (2004) Tumor galectinology: insights into the complex network of a family of endogenous lectins. Glycoconj J 20: 227-238.
3. Liu FT, Rabinovich GA, (2005) Galectins as modulators of tumour progression. Nat Rev Cancer 5: 29-41.
4. Massa SM, Cooper DN, Leffler H, Barondes SH, (1993) L-29, an endogenous lectin, binds to glycoconjugate ligands with positive cooperativity. Biochemistry 32: 260-267.
5. Leffler H, Carlsson S, Hedlund M, Qian Y, Poirier F, (2004) Introduction to galectins. Glycoconj J 19: 433-440.
6. Nakahara S, Oka N, Wang Y, Hogan V, Inohara H, et al. (2006) Characterization of the nuclear import pathways of galectin-3. Cancer Res 66: 9995-10006.
7. Nakahara S, Hogan V, Inohara H, Raz A, (2006) Importin-mediated nuclear translocation of alectin-3. J Biol Chem 285: 39649-39659.
8. Hughes RC, (1999) Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim Biophys Acta 1473: 172-185.
9. Camby I, Mercier ML, Lefranc F, Kiss R, (2006) Galectin-1: a small protein with major functions. Glycobiology 16: 137-157.
10. Ochieng J, Furtak V, Lukyanov P, (2004) Extracellular functions of galectin-3. Glycoconjugat J 19: 527-535.
11. Jeschke U, Karsten U, Wiest I, Schulze S, Kuhn C, et al. (2006) Binding of galectin-1 (gal-1) to the Thomsen-Friedenreich (TF) antigen on trophoblast cells and inhibition of proliferation of trophoblast tumor cells in vitro by gal-1 or an anti-TF antibody. Histochem Cell Biol 126: 437-444.
12. Yu LG, Andrews N, Zhao QC, McKean D, Williams JF, et al. (2007) Galectin-3 interaction with Thomsen-Friedenreich disaccharide on cancer-associated MUC1 causes increased cancer cell endothelial adhesion. J Biol Chem 282: 773-781.
13. Zhao QC, Barclay M, Hilkens J, Guo XL, Barrow H, et al. (2010) Interaction between circulating galectin-3 and cancer-associated MUC1 enhances tumour cell homotypic aggregation and prevents anoikis. Mol Cancer 9: 154-165.
14. Senapati S, Chaturvedi P, Chaney WG, Chakraborty S, Gnanapragassam VS, et al. (2011) Novel interaction of MUC4 and galectin: potential pathobiological implications for metastasis in lethal pancreatic cancer. Clin Cancer Res 17: 267-274.
15. Zhao Q, Guo X, Nash GB, Stone PC, Hilkens J, et al. (2009) Circulating galectin-3 promotes metastasis by modifying MUC1 localization on cancer cell surface. Cancer Res 69: 6799-6806.
16. Yu LG, (2007) The oncofetal Thomsen-Friedenreich carbohydrate antigen in cancer progression. Glycoconj J 24: 411-420.
17. Springer GF, (1997) Immunoreactive T and Tn epitopes in cancer diagnosis, prognosis, and immunotherapy. J Mol Med 75: 594-602.
18. Solvin SF, Ragupathi G, Musselli C, Fernandez C, Diani M, et al. (2005) Thomsen-Friedenreich (TF) antigen as a target for prostate cancer vaccine: clinical trial results with TF cluster (c)-KLH plus QS21 conjugate vaccine in patients with biochemically relapsed prostate cancer. Cancer Immunol Immunother 54: 694-702.
19. Walser PJ, Haebel PW, Kunzler M, Sargent D, Kues U, et al. (2004) Structure and functional analysis of the fungal galectin CGL2. Structure 12: 689-702.
20. Nagae M, Nishi N, Murata T, Usui T, Nakamura T, et al. (2006) Crystal structure of the galectin-9 N-terminal carbohydrate recognition domain from Mus musculus reveals the basic mechanism of carbohydrate recognition. J Biol Chem 281: 35884-35893.
21. Feng L, Sun H, Zhang Y, Li DF, Wang DC, (2010) Structural insights into the recognition mechanism between an antitumor galectin AAL and the Thomsen-Friedenreich antigen. Faseb J 24: 3861-3868.
22. López-Lucendo MF, Solís D, André S, Hirabayashi J, Kasai K-I, et al. (2004) Growth-regulatory human galectin-1: crystallographic characterisation of the structural changes induced by single-site mutations and their impact on the thermodynamics of ligand binding. J Mol Biol 343: 957-970.
23. Lobsanov YD, Gitt MA, Leffler H, Barondes SH, Rini JM, (1993) X-ray crystal structure of the human dimeric S-lac Lectin, L-14-II, in complex with lactose at 2.9-Å resolution. J Biol Chem 268: 27034-27038.
24. Liao DI, Kapadia G, Ahmed H, Vasta GR, Herzberg O, (1994) Structure of S-lectin, a developmentally regulated vertebrate b-galactosidebinding protein. Proc Natl Acad Sci U S A 91: 1428-1432.
25. Collins PM, Hidari KIPJ, Blanchard H, (2007) Slow diffusion of lactose out of galectin-3 crystals monitored by X-ray crystallography: possible implications for ligand-exchange protocols. Acta Cryst 63: 415-419.
26. Seetharaman J, Kanigsberg A, Slaaby R, Leffler H, Barondes SH, et al. (1998) X-ray crystal structure of the human galectin-3 carbohydrate recognition domain at 2.1-A resolution. J Biol Chem 273: 13047-13052.
27. Diehl C, Engström O, Delaine T, Håkansson M, Genheden S, et al. (2010) Protein flexibility and conformational entropy in ligand design targeting the carbohydrate recognition domain of galectin-3. J Am Chem Soc 132: 14577-14589.
28. Sörme P, Arnoux P, Kahl-Knutsson B, Leffler H, Rini JM, et al. (2005) Structural and thermodynamic studies on cation-Pi interactions in lectin-ligand complexes: high-affinity galectin-3 inhibitors through fine-tuning of an arginine-arene interaction. J Am Chem Soc 127: 1737-1743.
29. Nesmelova IV, Ermakova E, Daragan VA, Pang M, Menéndez M, et al. (2010) Lactose binding to galectin-1 modulates structural dynamics, increases conformational entropy, and occurs with apparent negative cooperativity. J Mol Biol 397: 1209-1230.
30. André S, Kaltner H, Lensch M, Russwurm R, Siebert HC, et al. (2005) Determination of structural and functional overlap/divergence of five proto-type galectins by analysis of the growth-regulatory interaction with ganglioside GM1 in silico and in vitro on human neuroblastoma cells. Int J Cancer 114: 46-57.
31. Bianchet MA, Ahmed H, Vasta GR, Amzel LM, (2000) Soluble β-galactosyl-binding lectin (galectin) from Toad Ovary: crystallographic studies of two protein-sugar complexes. Proteins 40: 378-388.
32. Bourne Y, Bolgiano B, Liao DI, Strecker G, Cantau P, et al. (1994) Crosslinking of mammalian lectin (galectin-1) by complex biantennary saccharides. Nature Struct Biol 1: 863-870.
33. Cumpstey I, Carlsson S, Leffler H, Nilsson UJ, (2005) Synthesis of a phenyl thio-β-D-galactopyranoside library from 1,5-difluoro-2,4-dinitrobenzene: discovery of efficient and selective monosaccharide inhibitors of galectin-7. Org Biomol Chem 3: 1922-1932.
34. Tejler J, Skogman F, Leffler H, Nilsson UJ, (2007) Synthesis of galactose-mimicking 1H-(1,2,3-triazol-1-yl)-mannosides as selective galectin-3 and 9N inhibitors. Carbohydr Res 342: 1869-1875.
35. Rossmann MG, van Beek CG, (1999) Data processing. Acta Crystallogr D Biol Crystallogr 55: 1631-1640.
36. Laskowski RA, MacArthur MW, Moss DS, Thornton JM, (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26: 283-291.
37. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
38. Jones TA, Zou JY, Cowan SW, Kjeldgaard M, (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst A47: 110-119.